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08/10/2005 04:11 PMMicrobiology in Yellowstone National Park

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David M. Ward is aprofessor at theDepartment ofMicrobiology, MontanaState University,Bozeman.

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Microbiology in Yellowstone National Park

Yellowstone, a hotspot for unusual research in microbiology, also provides a setting for outreacheducation

David M. WardAmerican Society for Microbiology

Originally published in ASM News , the News Magazine of the American Society for Microbiology - March 1998, Vol. 64, No. 3, pages 141-146

Yellowstone National Park plays host to numerous microbiological research projects — officially 23,according to the 1996 Investigators' Annual Reports. However, once categories such as aquatic ecology,the study of brucellosis and other wildlife diseases, environmental education, geochemistry and geothermalsystems, and vegetation are included, the total came to at least 35 in 1996. Research projects in otherscientific disciplines, including geochemistry, geology and environmental monitoring, fire impacts, and evenstudies of ungulates such as bison and elk, or of other mammals such as bears and wolves, are far fewerin overall numbers.

Yellowstone is one place where the importance ofmicroorganisms is immediately noticed. Despite the park’scharismatic megafauna, plentiful examples of fire’s impact onmegaflora, and its renowned geothermal features,Yellowstone is one place where the importance ofmicroorganisms is immediately noticeable — even if not fullyappreciated. As pointed out by my former researchassociate, Niels Ramsing of the University of Åarhus inDenmark, few who come to Yellowstone ever see a bear orwolf, while nearly everyone sees — but rarely appreciates — microorganisms that thrive in near-boilingwater. If appropriately in-formed, however, some of the 3 million annual tourists may begin to ponder whythese microorganisms live in water too hot for humans, why they exhibit more genetic diversity than allplants and animals, and that they may well represent the kinds of organisms from which all organisms,including plants and animals, evolved.

Meanwhile, an avid contingent of park administrators and visitors with scientific training already areconsiderably interested in Yellowstone’s microorganisms. On one level, this interest reflects a growingfascination with the opportunities for both academic and industrial microbiology research at Yellowstone.At another, it reflects concerns about how this research activity influences management of the park’smicrobiological resources. Beyond that, park officials, researchers, and educators also recognize that thenoteworthy microbiota present opportunities for changing the way the public thinks about microorganisms.

Extensive Research Raises Questions for Park Officials

Most of the more than 60 investigators conducting research inYellowstone Park are from universities and similar research institutes.Many others come from government agencies with basic researchinterests, such as the National Aeronautics and Space Administration



The effluent channel of TwinButte Vista Spring, a typicalalkaline siliceous spring(background) withcyanobacterial mat inforeground. Note "V-shaped"green coloration, which marksupper temperature limit ineffluent channel (ca. 74ºC).

interests, such as the National Aeronautics and Space Administration(NASA); with industrial or applied research interests, such as the IdahoNational Energy Laboratory, the National Renewable EnergyLaboratory, and the Alberta Research Council; or with natural resourcemanagement interests, including the U.S. Geological Survey and theNational Park Service.

Of greatest concern to park managers worried about preserving theintegrity of the park environment are the 11 projects sponsored bybiotechnology companies, whose interests revolve around Yellowstone’sthermophilic microorganisms and their potential to yield thermostableenzymes or unusual metabolites. The steadily growing interest in furtherexploiting such park resources faces officials who manage them with aserious challenge.

To assess available information about Yellowstone thermophiles andto discuss some of the broader issues involved in managing the park'smicrobial resources, park officials asked Anna-Louise Reysenbach ofRutgers University to organize a meeting several years ago. Thatconference, "Biodiversity, Ecology and Evolution of Thermophiles inYellowstone National Park: Overview and Issues," held at Old Faithful inSeptember 1995, helped to frame many of these complex issues.

In 1996, the World Foundation for Environment and Development(WFED), a non-profit organization based in Washington, D.C., thatspecializes in resolving environmental disputes, convened a follow-upworkshop for park managers and academic and industry scientists. Byholding that workshop in Costa Rica, participants experienced first-hand how that country, through theINBIO (Instituto Nacional de Bioversidad) organization, promotes a new paradigm for conservation that isbased on renewable resource use by private industry combined with information flow to and profit sharingwith the public.

Based on such discussions and the development of strategies since the two conferences, officials fromYellowstone National Park entered into a prototype relationship with Diversa Corp. of San Diego, Calif.This agreement exchanges access to thermophilic microbial resources for information learned frommolecular studies of microbial diversity in Yellowstone along with a share in profits through royalties,which are to be used to improve the management of park resources.

Main Microbiology Focus is Extremophiles

FIGURE 2

Close-up view of cyanobacterial matsample (Octopus Spring, ca. 60ºC),showing laminations that resemblethose found in stromatolites.



Microbiological research activities at Yellowstone intensified several decades ago. My Ph.D. mentorThomas D. Brock at the University of Wisconsin, Madison, and other microbiologists, notably Richard W.Castenholz at the University of Oregon, Eugene, established a tradition at Yellowstone through theirintensive efforts in the 1960s and 1970s to cultivate thermophiles and to conduct direct ecophysiologicalstudies on indigenous thermophilic microbial communities. That research laid a solid foundation to ourknowledge of the diversity, ecology, and physiology of thermophilic microorganisms.

Though the majority of the microbiological research projects under way in Yellowstone involves basicstudies on extremophiles, a few do not. For instance, two projects address the possibility of brucellosistransmission from bison to cattle (see p. 132). Two other projects involve microbe-plant associations, withone focusing on microorganisms in the rhizosphere of plants adapted to acid and thermal soils and theother on microorganisms which grow as epiphytes on plant surfaces. Several of the applied microbiologyprojects involving extremophiles are concerned with catalytic processes, such as denitrification, fossil fuelmodification, chromate reduction, metal decontamination, metal resistance, and desulfurization.

FIGURE 3

Pink streamers of filamentous bacteria at ca. 85ºCat Octopus Spring.

Most of the basic studies on microorganisms from Yellowstone involve prokaryotes. However, a fewprojects focus on eukaryotic diatoms and fungi, and one project focuses on thermophilic viruses. Eventhough several of the unusual thermoacidophiles, such as Sulfolobus acidocaldarius, obtained fromYellowstone hot springs are members of the archaea, only two current projects specifically focus onmembers of this evolutionarily novel group of microorganisms. Most Yellowstone-based microbiologicalresearch projects focus on bacteria, including cyanobacteria, anoxygenic phototrophs, and aerobic andanaerobic chemoorganotrophs. Following the tradition established by Brock and Castenholz, these rangefrom descriptions of new isolates to studies of their physiology and genetics to ecophysiological studies oftheir activities in situ. For example, one of the studies from my laboratory involves detailed analysis ofphotosynthesis within cyanobacterial mat populations. Robert Lindstrom, a staff member of Yellowstone’sCenter for Resources and the park’s microbiology liaison officer, is compiling a database derived fromsuch studies of the thermophilic microorganisms of Yellowstone.

Molecular Methods Being Used To Explore Diversity of Uncultivated Yellowstone Microbes

The remarkable discoveries about evolution made by Carl Woese of the University of Illinois and othermicrobiologists since the late 1970s have significantly affected research on extremophiles from habitatssuch as those in Yellowstone. For example, 16S rRNA-based molecular methods that played an integralrole in those discoveries are being used to analyze microorganisms that grow in hot spring habitats butresist cultivation in laboratories. Such analytical methods help to reveal the remarkable diversity of thesemicroorganisms that exists in nature.

The work of Woese and others led to the hypothesis that hyperthermophiles are among the earliestorganisms to have evolved. This hypothesis has become a major driving force behind the efforts of



Norman Pace of the University of California, Berkeley, and his collaborators to describe more fully themicrobial diversity in Yellowstone's most extreme thermal environments. They recently reported findingdiverse new lineages of archaea in a single hot spring source pool. Karl Stetter and his colleagues haveused novel cultivation approaches to bring some of these microorganisms from hot spring habitats intopure culture.

Similarly, Reysenbach and her colleagues at Rutgers University have discovered new descendants ofsome of the earliest known bacterial lineages, such as Thermotogales and Aquifexales, inhyperthermophilic "streamer" communities. They are conducting in situ ecophysiology studies that maysoon lead to cultivation of representative microorganisms from such communities.

Diversity Explained by Universal Principles of Ecology and Evolution

My students and I are using similar molecular approaches to study the evolutionary and ecologicalbasis for the diversity within some of these microbiological communities, such as the cyanobacterial matsfound in the alkaline siliceous Octopus Spring in Yellowstone. The diversity of uncultivated prokaryoteswithin such microbial communities is truly remarkable. For example, of 31 unique 16S rRNA sequencesdetected in the Octopus Spring mat, none match the 16S rRNA sequence of any previously cultivatedisolate.

We have recently revised our estimates of diversity among the cyanobacteria dramatically upward. Adecade ago, when researchers observed a single morphotype microscopically and could cultivate only asingle genotype by standard methods, they reported that a single Synechococcus species made up themat. We now have detected at least 11 distinct cyanobacterial 16S rRNA sequences in the mat, and theirgenetic diversity rivals that found among all cyanobacteria.

Culture and molecular methods give such different views of community composition in large partbecause readily cultivated bacteria are "lab weeds," and thus we have had to learn how to exclude them tocultivate predominant species which are more difficult to grow.

As ecologists, we are trying to understand why all this diversity exists, how it is organized, and what itcontributes to overall community structure and function. Patterns of distribution of specific 16S rRNAsequences along environmental gradients clarify the relationship between 16S rRNA sequence diversityand organismic diversity, and we can see that bacteria obey ecological and evolutionary rules that apply toall species. For example, both cyanobacteria and green non-sulfur bacteria inhabiting the mat appear tohave undergone evolutionary radiations, much like Darwin's Galapagos finches, with species adapteddifferently to temperature and light. We are also beginning to see that diversity measurements based on16S rRNA sequences underestimate microbial species diversity.

According to Michael Kuhl and colleagues at the Max Planck Institute for Marine Microbial Ecology,Bremen, Germany, species diversity may be important to stabilizing guild activities within the community.They have observed that the cyanobacteria that coexist in the mat are adapted to different temperatures.These cyanobacteria reduce the sensitivity of oxygenic photosynthesis, the guild activity to which theycontribute, to temperature fluctuations.

Park Provides Insights into the History of Life on Earth (and Mars?)

Yellowstone provides settings that are of special value to microbiologists who are addressing questionsof intense interest in exobiology. For example, David Des Marais, Jack Farmer, and their collaborators atNASA Ames Research Center in Moffett Field, Calif., speculate that life existed on early Mars ingeothermal settings. To model martian environments and the evidence of microbial life that might be foundthere, Des Marais and Farmer are studying how thermophilic microbial communities occur in relation to thegeothermal landscape and how they are preserved as fossils. Such studies will influence site selection andsample collection on future missions to Mars.

Other scientists are working in Yellowstone to probe other issues concerning ancient microbiology. Forinstance, I am collaborating with organic geochemists Geoffrey Eglinton at Bristol University, in Bristol,United Kingdom, and Jan de Leeuw at the Netherlands Institute for Sea Research, Texel, the Netherlands,



studying the relationship between mat-forming microorganisms and their recalcitrant organic remains. Weare trying to understand better how these "chemical fossils" and their stable isotope signatures arepreserved in mat communities, considered to be analogs of stromatolites, the predominant fossils of thePrecambrian era. Some efforts involve investigating Chloroflexus mats found in sulfide-rich springs inYellowstone Park. These anoxygenic phototrophs seem to have arisen before cyanobacteria. If true, themats they formed would predate cyanobacterial mats.

Similarly, Beverly Pierson from the University of Puget Sound in Tacoma, Wash., is investigating therelationship between photosynthetic prokaryotes and minerals found in iron-rich springs. She hopes todetermine whether banded iron formations constitute a "chemical finger-print" of oxygen derived fromcyanobacterial photosynthesis.

Yellowstone Also Provides Valuable Setting for Educators

Educators find Yellowstone a valuable setting for science teaching projects. Included in this categoryare high school student projects, a workshop for high school educators, an undergraduate programsponsored by the National Science Foundation, and a microbial diversity field course for graduatestudents.

Yellowstone is also being used to educate the public through several outreach projects. For example,WFED is coordinating production of a video for educating park visitors about the microbial life associatedwith the many thermal features of the park. Meanwhile, Crest Films of Santa Monica, Calif., is producing afilm on western national parks for the Discovery Channel that includes a segment on Yellowstone’scharismatic microbiota. Kurtis Productions, Ltd. of Chicago, Ill., is producing an hour-long New Explorer'sprogram, "From Yellowstone to Mars," for the Arts and Education Network that features thermophiles. Bothprograms are scheduled to air in spring 1998, the latter program being tentatively scheduled for 2 April.

WFED, in conjunction with ASM, is producing a guidebook for the Midway Geyser Basin that willintroduce tourists to the microbiological features there. These kinds of projects have the potential tochange the way the public thinks about microorganisms, providing a more comprehensive and naturalisticview of microorganisms instead of the conventional view of microbes as "germs."

This article is dedicated to Yellowstone’s "chief geyser gazer," Rick Hutchinson, whose tragic death lastyear will be a setback to all microbiologists working in the park. A man of numbers, Rick wondered aboutthe number of days till Christmas, about the number of snow fleas beneath his skis, and about the diverseunexplored thermal habitats of Yellowstone that will undoubtedly occupy the interests of microbiologists aswe proceed without his guidance.

ACKNOWLEDGMENT

I thank Bob Lindstrom for providing the 1996 Investigators' Annual Reports and a list of individuals andcorporations currently conducting microbiology research projects in the park, which I used as primaryreferences for this article.

SUGGESTED READING

Brock, T. D. 1978. Thermophilic microorganisms and life at high temperatures. Springer-Verlag, NewYork.

Cady, S. L., and J. D. Farmer. 1996. Fossilization processes in siliceous thermal springs: trends inpreservation along thermal gradients, p. 150–173. In G. R. Bock and J. A. Goode (ed.) Evolution ofhydrothermal systems on Earth (and Mars?). John Wiley, Chichester, United Kingdom (CIBA FoundationSymp. 202).

Pace, N. R. 1997. A molecular view of microbial diversity and the biosphere. Science 276:734–740.

Reysenbach, A. L., G. S. Wickham, and N. R. Pace. 1994. Phylogenetic analysis of thehyperthermophilic pink filament community in Octopus Spring, Yellowstone National Park. Appl. Environ.



Microbiol. 60:2113–2119.

Reysenbach, A.-L. (ed.). Biodiversity, ecology and evolution of thermophiles in Yellowstone NationalPark: overview and issues, in press. Plenum Press, New York.

Walter, M. R., and D. J. Des Marais. 1993. Preservation of biological information in thermal springdeposits: developing a strategy for the search for fossil life on Mars. Icarus 101:129–143.

Ward, D. M., M. M. Bateson, and J. W. de Leeuw. Use of 16S rRNA, lipid and naturally preservedcomponents of hot spring mats and microorganisms to help interpret the record of microbial evolution. InA.-L. Reysenbach (ed.), Biodiversity, ecology and evolution of thermophiles in Yellowstone National Park:overview and issues, in press. Plenum Press, New York.

Ward, D. M., and R. W. Castenholz. Cyanobacteria in geothermal habitats. In M. Potts and B. Whitton(ed.), Ecology of cyanobacteria, in press. Kluwer Press, Amsterdam.

Ward, D. M., M. J. Ferris, S. C. Nold, and M. M. Bateson. Microbial biodiversity within hot springcyanobacterial mat communities: an evolutionary ecology view. Microbiol. Mol. Biol. Rev., submitted.

Yellowstone Center for Resources. 1997. Investigators’ Annual Reports, Yellowstone National Park.Yellowstone Center for Resources, Yellowstone National Park, Wyo.

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